Hemibiotrophs

(Redirected from Hemibiotrophic)

Hemibiotrophs are the spectrum of plant pathogens, including bacteria, oomycete and a group of plant pathogenic fungi that keep its host alive while establishing itself within the host tissue, taking up the nutrients with brief biotrophic-like phase.[1][2] It then, in later stages of infection switches to a necrotrophic life-style, where it rampantly kills the host cells, deriving its nutrients from the dead tissues.[3]

This mode of interaction, in which initial biotrophy followed by a switch to necrotrophy, has been observed in the fungal model Magnaporthe oryzae (rice blast fungus) and other pathogens such as many Colletotrichum spp. (often called anthracnose diseases, e.g. Colletotrichum lindemuthianum), Southern corn leaf blight (Bipolaris maydis) and, Zymoseptoria tritici (syn. Mycosphaerella graminicola, leaf blotch of wheat).[4][5][6] Collectively, they represent some of the most destructive plant parasites, causing huge economic losses, threatening global food security.[7]

A spectrum of hemibiotrophic plant pathogens, including the bacterium Pseudomonas syringae and the oomycete Phytophthora infestans (potato blight), also exhibit characteristics of both biotrophs and necrotrophs and thus are called hemibiotrophs, depending on the stages of their life cycle.[citation needed]

Life style

edit

In contrast to biotrophs, hemibiotrophs have dual life-styles. The initial biotrophic life-style of hemibiotrophs causes minimum damage to the plant tissues, while the fungus obtains nutrients from living plant tissues [8] Hemibiotrophic fungi require living plant tissue to survive to complete their life cycle.

Most fungal hemibiotrophs develop haustoria, whereas some produce intracellular hyphae to acquire nutrients from the host cytoplasm.[9][10] However, in the hemibiotrophic life-style the pathogen later breaks down host cell walls through secretion of hydrolytic enzymes and feeds on the released nutrients.[8][11] These hydrolytic enzymes and toxins are synthesized during the later necrotrophic phase. They also produce extracellular hyphae between the host cells to facilitate nutrient assimilation.[8][9] Plant pathogenic fungi produce and secrete many so‐called effector proteins that interact with the host and play an important role in virulence.

The rice blast fungus Magnaporthe oryzae[12] and Colletotrichum species are generally considered to be hemibiotrophs.[8][1][13] Three hemibiotrophic species, Colletotrichum pisicola, C. vignae and C. destructivum belong to the Colletotrichum destructivum complex. Fusarium oxysporum  is the cause of fusarium wilt disease and Moniliophthora roreri, which causes frosty pod rot disease of cacao, are hemibiotrophs that affect many agricultural and floricultural crops worldwide [14][15][16]

In the early stages of infection, the pathogens proliferate asymptomatically in the host by suppressing programmed cell death (PCD) or thwarting host defense responses, but in the later stages of infection they undergo a physiological transition from asymptomatic biotrophic growth to a highly destructive necrotrophic phase. Hemibiotrophic bacteria are known to secrete a range of so-called effector proteins, including transcription factors and others with enzymatic activities, into host cells via the type III secretion system (T3SS)[17] whereupon they suppress PCD and other host defenses.[18][19]

Hemibiotrophy genes

edit

Studies indicate that fungal hemibiotrophic C. lindemuthianum species undergo two distinct phases during host invasion. Initially, the biotrophic phase involves generating intracellular hyphae within intact plant cells. Subsequently, the necrotrophic phase occurs where extracellular hyphae penetrate cellular boundaries, traversing plasmodesmata and spreading between host cells.

The suggestion that these fungi undergo a distinct metabolic switch from biotrophic to necrotrophic growth was boosted by the discovery of a gene that functions between the biotrophic and necrotrophic phases. The gene CLTA1 encodes a GAL4‐like transcriptional activator, which is consistent with a role in reprogramming metabolism. It is clear that all pathogens are obliged to alter metabolic fluxes in numerous ways upon penetration to prepare for proliferation. This is a key postulated attribute of the hemibiotrophs and seems to be a priority subject for study.[4]

Life cycle of hemibiotrophs

edit

The hemibiotrophic life cycle involves an initial biotrophic phase and later a necrotrophic phase.[8][9] Colletotrichum lindemuthianum is a hemibiotrophic fungus on beans (common bean anthracnose).[4][20][21] Conidia then, on the host surface, germinate and differentiate to form a melanized infection structure devoted to mechanical penetration of the epidermal cells.[12][21] After the penetration step, the infection cycle is characterized by two successive phases. In the first phase, lasting 3 to 4 days, the fungus grows biotrophically inside the infected epidermal cells. During this phase, referred to as the biotrophic phase, the appressoria develops into a primary penetration hypha, which is surrounded by the invaginated plant plasma membrane, during this phase the penetrated host cell remains alive with minimum damage. The second phase, which corresponds to the appearance of symptoms, is completed 6 to 8 days after inoculation. During this phase, the necrotrophic phase, the fungus develops secondary hyphae that grow both intracellularly and intercellularly and thus acts as a typical necrotrophic pathogen. During the necrotrophic phase the fungus secretes cell wall-degrading enzymes that break down the host cell wall. After a few days the plant cell membrane disintegrates and ultimately the host cell dies.[12][17] Thereafter the fungus grows as a necrotroph.

Another hemibiotroph is Moniliophthora roreri, which causes frosty pod rot on Theobroma sp. (Cacao).[21] It produces meiospores, via meiosis, from the modified basidium.[21][22] These spores are important as dispersal agents, for infection and survival.[22] Meiospores germinate and produce hyphae made up of haploid cells throughout the biotrophic phase. The necrotrophic phase is thought to start from the formation of dikaryotic hyphae and continues until sporulation on the pod surface.[13][22][23]

References

edit
  1. ^ a b Mendgen, Kurt; Hahn, Matthias (August 2002). "Plant infection and the establishment of fungal biotrophy". Trends in Plant Science. 7 (8): 352–356. Bibcode:2002TPS.....7..352M. doi:10.1016/s1360-1385(02)02297-5. ISSN 1360-1385. PMID 12167330.
  2. ^ Lee, Sang-Jik; Rose, Jocelyn K.C. (June 2010). "Mediation of the transition from biotrophy to necrotrophy in hemibiotrophic plant pathogens by secreted effector proteins". Plant Signaling & Behavior. 5 (6): 769–772. Bibcode:2010PlSiB...5..769L. doi:10.4161/psb.5.6.11778. ISSN 1559-2324. PMC 3001586. PMID 20400849.
  3. ^ Horbach, Ralf; Navarro-Quesada, Aura Rocio; Knogge, Wolfgang; Deising, Holger B. (January 2011). "When and how to kill a plant cell: Infection strategies of plant pathogenic fungi". Journal of Plant Physiology. 168 (1): 51–62. Bibcode:2011JPPhy.168...51H. doi:10.1016/j.jplph.2010.06.014. ISSN 0176-1617. PMID 20674079.
  4. ^ a b c Perfect, Sarah E.; Green, Jonathan R. (March 2001). "Infection structures of biotrophic and hemibiotrophic fungal plant pathogens". Molecular Plant Pathology. 2 (2): 101–108. doi:10.1046/j.1364-3703.2001.00055.x. ISSN 1464-6722. PMID 20572997.
  5. ^ Kumar, Jagdish; Schäfer, Patrick; Hückelhoven, Ralph; Langen, Gregor; Baltruschat, Helmut; Stein, Elke; Nagarajan, Subramaniam; Kogel, Karl-Heinz (July 2002). "Bipolaris sorokiniana , a cereal pathogen of global concern: cytological and molecular approaches towards better control‡". Molecular Plant Pathology. 3 (4): 185–195. doi:10.1046/j.1364-3703.2002.00120.x. ISSN 1464-6722. PMID 20569326.
  6. ^ Shetty, Nandini P.; Mehrabi, Rahim; Lütken, Henrik; Haldrup, Anna; Kema, Gert H. J.; Collinge, David B.; Jørgensen, Hans Jørgen Lyngs (May 2007). "Role of hydrogen peroxide during the interaction between the hemibiotrophic fungal pathogen Septoria tritici and wheat". New Phytologist. 174 (3): 637–647. doi:10.1111/j.1469-8137.2007.02026.x. ISSN 0028-646X. PMID 17447918.
  7. ^ Koeck, Markus; Hardham, Adrienne R.; Dodds, Peter N. (2011-09-14). "The role of effectors of biotrophic and hemibiotrophic fungi in infection". Cellular Microbiology. 13 (12): 1849–1857. doi:10.1111/j.1462-5822.2011.01665.x. ISSN 1462-5814. PMC 3218205. PMID 21848815.
  8. ^ a b c d e Latijnhouwers, Maita; de Wit, Pierre J.G.M.; Govers, Francine (October 2003). "Oomycetes and fungi: similar weaponry to attack plants". Trends in Microbiology. 11 (10): 462–469. doi:10.1016/j.tim.2003.08.002. ISSN 0966-842X. PMID 14557029.
  9. ^ a b c OLIVER, RICHARD P.; IPCHO, SIMON V. S. (July 2004). "Arabidopsis pathology breathes new life into the necrotrophs-vs.-biotrophs classification of fungal pathogens". Molecular Plant Pathology. 5 (4): 347–352. doi:10.1111/j.1364-3703.2004.00228.x. ISSN 1464-6722. PMID 20565602.
  10. ^ Divon, Hege H.; Fluhr, Robert (January 2007). "Nutrition acquisition strategies during fungal infection of plants". FEMS Microbiology Letters. 266 (1): 65–74. doi:10.1111/j.1574-6968.2006.00504.x. ISSN 0378-1097. PMID 17083369.
  11. ^ Kabbage, Mehdi; Yarden, Oded; Dickman, Martin B. (April 2015). "Pathogenic attributes of Sclerotinia sclerotiorum : Switching from a biotrophic to necrotrophic lifestyle". Plant Science. 233: 53–60. Bibcode:2015PlnSc.233...53K. doi:10.1016/j.plantsci.2014.12.018. ISSN 0168-9452. PMID 25711813.
  12. ^ a b c Kankanala, Prasanna; Czymmek, Kirk; Valent, Barbara (February 2007). "Roles for Rice Membrane Dynamics and Plasmodesmata during Biotrophic Invasion by the Blast Fungus". The Plant Cell. 19 (2): 706–724. doi:10.1105/tpc.106.046300. ISSN 1040-4651. PMC 1867340. PMID 17322409.
  13. ^ a b Latunde-Dada, A. O.; Lucas, J. A. (2007-03-12). "Localized hemibiotrophy in Colletotrichum: cytological and molecular taxonomic similarities among C. destructivum, C. linicola and C. truncatum". Plant Pathology. 56 (3): 437–447. doi:10.1111/j.1365-3059.2007.01576.x. ISSN 0032-0862.
  14. ^ Meinhardt, Lyndel W; Costa, Gustavo Gilson; Thomazella, Daniela PT; Teixeira, Paulo José PL; Carazzolle, Marcelo; Schuster, Stephan C; Carlson, John E; Guiltinan, Mark J; Mieczkowski, Piotr; Farmer, Andrew; Ramaraj, Thiruvarangan (2014). "Genome and secretome analysis of the hemibiotrophic fungal pathogen, Moniliophthora roreri, which causes frosty pod rot disease of cacao: mechanisms of the biotrophic and necrotrophic phases". BMC Genomics. 15 (1): 164. doi:10.1186/1471-2164-15-164. ISSN 1471-2164. PMC 3948071. PMID 24571091.
  15. ^ Król, P.; Igielski, R.; Pollmann, S.; Kępczyńska, E. (May 2015). "Priming of seeds with methyl jasmonate induced resistance to hemi-biotroph Fusarium oxysporum f.sp. lycopersici in tomato via 12-oxo-phytodienoic acid, salicylic acid, and flavonol accumulation". Journal of Plant Physiology. 179: 122–132. Bibcode:2015JPPhy.179..122K. doi:10.1016/j.jplph.2015.01.018. ISSN 0176-1617. PMID 25867625.
  16. ^ Damm, U.; O'Connell, R.J.; Groenewald, J.Z.; Crous, P.W. (September 2014). "The Colletotrichum destructivum species complex – hemibiotrophic pathogens of forage and field crops". Studies in Mycology. 79: 49–84. doi:10.1016/j.simyco.2014.09.003. ISSN 0166-0616. PMC 4255528. PMID 25492986.
  17. ^ a b Alfano, James R.; Collmer, Alan (September 2004). "TYPE III SECRETION SYSTEM EFFECTOR PROTEINS: Double Agents in Bacterial Disease and Plant Defense". Annual Review of Phytopathology. 42 (1): 385–414. doi:10.1146/annurev.phyto.42.040103.110731. ISSN 0066-4286. PMID 15283671. S2CID 39907279.
  18. ^ Espinosa, Avelina; Alfano, James R. (November 2004). "Disabling surveillance: bacterial type III secretion system effectors that suppress innate immunity". Cellular Microbiology. 6 (11): 1027–1040. doi:10.1111/j.1462-5822.2004.00452.x. ISSN 1462-5814. PMID 15469432. S2CID 35641145.
  19. ^ Chisholm, Stephen T.; Coaker, Gitta; Day, Brad; Staskawicz, Brian J. (February 2006). "Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response". Cell. 124 (4): 803–814. doi:10.1016/j.cell.2006.02.008. ISSN 0092-8674. PMID 16497589. S2CID 10696351.
  20. ^ Dufresne, Marie; Perfect, Sarah; Pellier, Anne-Laure; Bailey, John A.; Langin, Thierry (September 2000). "A GAL4-like Protein Is Involved in the Switch between Biotrophic and Necrotrophic Phases of the Infection Process of Colletotrichum lindemuthianum on Common Bean". The Plant Cell. 12 (9): 1579–1589. doi:10.1105/tpc.12.9.1579. ISSN 1040-4651. PMC 149071. PMID 11006333.
  21. ^ a b c d Souza, E.A.; Camargo Jr., O.A.; Pinto, J.M.A. (2010). "Sexual recombination in Colletotrichum lindemuthianum occurs on a fine scale". Genetics and Molecular Research. 9 (3): 1759–1769. doi:10.4238/vol9-3gmr863. ISSN 1676-5680. PMID 20830667.
  22. ^ a b c Münch, Steffen; Lingner, Ulrike; Floss, Daniela S.; Ludwig, Nancy; Sauer, Norbert; Deising, Holger B. (January 2008). "The hemibiotrophic lifestyle of Colletotrichum species". Journal of Plant Physiology. 165 (1): 41–51. Bibcode:2008JPPhy.165...41M. doi:10.1016/j.jplph.2007.06.008. ISSN 0176-1617. PMID 17765357.
  23. ^ Evans, Harry C. (December 2007). "Cacao Diseases—The Trilogy Revisited". Phytopathology. 97 (12): 1640–1643. doi:10.1094/phyto-97-12-1640. ISSN 0031-949X. PMID 18943725.